Abstract
Testosterone (T) concentrations in many species are sensitive to seasonal changes and to changes in social conditions. However, the effect of the natural or endogenous T increase in the juvenile on their social behaviour is not well understood. In this study, T and behaviour were measured from the pro-social juvenile to the adult stage in semi-feral domestic fowl. During the pro-social phase T levels and the distance chicks maintained between each other, i.e. inter-individual distance (IID) were low. Then, as T increased, a corresponding increase in IID occurred and continued in males until dispersal to individual adult male territories. In the new and initially stable adult social structure, T declined and IID remained high, indicating a new behavioural mechanism was in place. Males first mated as T levels were declining. They were then challenged; then T increased, and then IID increased again. Adult male T levels fluctuate, being low or declining in a socially stable environment and increasing following a challenge, suggesting a regulatory or modulating role for T. The results are consistent with T having an endogenous role: in the juvenile, driving behavioural change towards adulthood, and in adulthood, a modulating role regulating social organisation.

Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Andrew RJ (1966) Precocious adult behaviour in the young chick. Anim Behav 14:485–500
Andrew RJ, Rogers LJ (1972) Testosterone, search behaviour and persistence. Nature 237:343–346
Bateson P (1981) Discontinuities in development and changes in the organization of play in cats. In: Immelmann K, Barlow GE, Petrinovich L, Main M (eds) Behavioural development: The Bielefeld Interdisciplinary Project. Cambridge University Press, UK, pp 281–295
Brockman DK, Whitten PL, Richard AF, Benander B (2001) Birth season testosterone levels in male Verreaux's sifiaka, (Propithecus verreauxi): insights into socio-demographic factors mediating seasonal testicular function. Behav Ecol Sociobiol 49:117–127
Chalmers NR (1987) Developmental pathways in behaviour. Anim Behav 35:659–674
Cockrem JF, Rounce JR (1994) Faecal measurements of oestradiol and testosterone allow the non-invasive estimation of plasma steroid concentrations in the domestic fowl. Br Poult Sci 35:433–443
Collias NE, Collias EC (1967) A field study of the red junglefowl in north-central India. Condor 69:360–386
Collias NE, Collias EC (1996) Social organization of a red junglefowl, Gallus gallus, population related to evolutionary theory. Anim Behav 51:1337–1354
Crawford RD (1990) Origin and history of poultry species. In: Crawford RD (ed) Poultry breeding and genetics. Elsevier, New York, pp 1–42
Douglis M (1948) Social factors influencing the hierarchies of the domestic hen: interactions between resident and part-time members of organised flocks. Physiol Zool 21:147–182
Eising CM, Eikenaar C, Schwabl H, Groothuis T (2001) Maternal androgens in black-headed gull Larus ridibundus eggs: consequences for chick development. Proc R Soc Lond B 268:839–846
Eising CM, Groothuis TG (2003) Yolk androgens and begging behaviour in black headed gull chicks: an experimental field study. Anim Behav 66:1027–1034
Fumihito A, Miyake T, Sumi S-I, Takada M, Ohno S, Kondo N (1994) One species of the red junglefowl, Gallus gallus gallus suffices as the matriarchic ancestor of all domestic breeds. Proc Natl Acad Sci U S A 91:12505–12509
Goymann W (2005) Noninvasive monitoring of hormones in bird droppings: physiological validation, sampling, extraction, sex differences and the influence of diet on hormone metabolite levels. Ann NY Acad Sci 1046:35–53
Hau M (2001) Timing of breeding in variable environments: tropical birds as model systems. Horm Behav 40:281–290
Hunt KE, Hahn TP, Wingfield JC (1997) Testosterone implants increase song but not aggression in male Lapland longspurs. Anim Behav 54:1177–1192
Johnsen TS, Zuk M (1995) Testosterone and aggression in male red jungle fowl. Horm Behav 29:593–598
Kent JP (1992) Maternal aggression and inter-individual distance in the broody hen (Gallus gallus). Behav Proc 27:37–44
Kent JP, McElligott AG, Budgey HV (1997) Ground-roosting in domestic fowl (Gallus gallus domesticus) in The Gambia: the anticipation of night. Behav Proc 39:271–278
Ketterson ED, Nolan V Jr (1992) Hormones and life histories: an integrative approach. Am Nat Suppl 140:33–62
Kruijt JP (1964) Ontogeny of social behaviour in Burmese red junglefowl (Gallus gallus spadiceus). Behav Suppl 12:1–195
Lehner PN (1979) Handbook of ethological methods. Cambridge University Press, Cambridge
Ligon DJ, Zwartjes WZ (1995) Female red junglefowl choose to mate with multiple males. Anim Behav 49:127–135
Lincoln GA (1971) The seasonal reproductive changes in the red deer stag (Cervus elaphus). J Zool (London) 163:105–123
Lynn SE, Houtman AM, Weathers WW, Ketterson ED, Nolan V Jr (2000) Testosterone increases activity but not daily energy expenditure in captive male dark-eyed juncos, Junco hyemalis. Anim Behav 60:581–587
Lynn SE, Hayward LS, Benowitz-Fredericks Z, Wingfield JC (2002) Behavioural insensitivity to supplementary testosterone during the parental phase in the chestnut-collared longspur, Calcarius ornatus. Anim Behav 63:795–803
Marler P (1956) Studies of fighting in chaffinches (3) proximity as a cause of aggression. Anim Behav 4:23–29
Ottinger MA (1983) Hormonal control of reproductive behaviour in the avian male. Poul Sci 62:1690–1699
Owens IPF, Short RV (1995) Hormonal basis of sexual dimorphism in birds: implications for new theories of sexual selection. Tree 10:44–47
Pellegrini AD (2004) Sexual segregation in childhood: a review of evidence for two hypotheses. Anim Behav 68:435–443
Pizzari T, Cornwallis CK, Lovlie H, Jakobsson S, Birkhead TR (2003) Sophisticated sperm allocation in male fowl. Nature 426:70–74
Ronayne E, Enright WJ, Roche JF (1993) Effects of continuous administration of gonadotrophin-releasing hormone (GnRH) or a potent GnRH analogue on blood luteinising hormone and testosterone concentrations in prepubertal bulls. Dom Anim Endocrinol 10:179–189
Ruckstuhl KE, Neuhaus P (2002) Sexual segregation in ungulates: a comparative test of three hypotheses. Biol Rev 77:77–96
Ruckstuhl KE, Neuhaus P (2005) Activity asynchrony and social segregation. In: Ruckstuhl KE, Neuhaus P (eds) Sexual segregation in vertebrates: ecology of the two sexes. Cambridge University Press, Cambridge, pp 165–179
Sapolsky RM (1983) Endocrine aspects of social instability in the olive baboon Papio anabis. Am J Primatol 5:365–379
Sapolsky RM (1993) The physiology of dominance in stable versus unstable social hierarchies. In: Manson WA, Mendoza SP (eds) Primate social conflict. State University of New York Press, Albany, NY, pp 179–204
Schwabl H (1996) Maternal testosterone in the avian egg enhances postnatal growth. Comp Biochem Physiol 114:271–276
Sharp PJ, Cuthbert J, Wells JW (1977) Variations in stored and plasma concentrations of androgens and luteinising hormone during sexual development in the cockerel. J Endocrinol 74:467–476
Sharp PJ, Gow CB (1983) Neuroendocrine control of reproduction in the cockerel. Poult Sci 62:1671–1675
Silver R (1992) Environmental factors influencing hormone secretion. In: Becker JB, Breedlove SM, Crews D (eds) Behavioural endocrinology. MIT Press, Cambridge, MA
Sockman KW, Schwabl H (2000) Yolk androgens reduce offspring survival. Proc R Soc Lond B 267:1451–1456
Wikelski M, Hau M, Wingfield JC (1999) Social instability increases plasma testosterone in a year round territorial neotropical bird. Proc R Soc Lond B 266:551–556
Wingfield JC (1984a) Short term changes in plasma levels of hormones during establishment and defence of a breeding territory in male song sparrows, Melospiza melodia. Horm Behav 19:174–187
Wingfield JC (1984b) Environmental and endocrine control of reproduction in the song sparrow, Melospiza melodia. II. Agonistic interactions as environmental information stimulates secretion of testosterone. Gen Comp Endocrinol 56:417–424
Wingfield JC (1994) Hormone–behaviour interaction and mating systems in male and female birds. In: Short RV, Bababan E (eds) The differences between the sexes. Cambridge University Press, Cambridge, UK, pp 303–330
Wingfield JC, Farner DS (1993) Endocrinology of reproduction in wild species. In: Farner DS, King JR, Parkes KC (eds) Avian biology. Academic, New York, pp 163–327
Wingfield JC, Hegner RE, Dufty AM Jr, Ball GF (1990) The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating systems and breeding strategies. Am Nat 136:829–846
Wingfield JC, Jacobs J, Hillgarth N (1997) Ecological constraints and the evolution of Hormone-Behaviour Interrelationships. Ann New York Acad Sci 807:22–41
Acknowledgements
We wish to thank Prof. R.J. Andrew, University of Sussex and Prof. T. Bolger, University College Dublin for comments on various drafts of this paper and Seamus McDonnell for assistance with extractions and assay work. J. P. K. conceived the project, provided facilities for the fowl, made links with the relevant departments, took part in about 40% behavioural observations and wrote the paper with K.M. and F.B. and collected faecal samples with K.M., who cared for birds, and did 60% behavioural observations. K.M. did the graphics and assisted N.H. who did extractions and the radioimmunoassays. F.B. did analysis on T data assisted by K.M. T.J.H. provided valued guidance at all stages of the work. We would wish to thank the editor and eight reviewers for comments and advice that we much appreciate. This research complies with the current laws of this country, and the ethical guidelines for the use of animals in research as outlined by The Association for the Study of Animal Behaviour.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kent, J.P., Murphy, K.J., Bannon, F.J. et al. Testosterone: from initiating change to modulating social organisation in domestic fowl (Gallus gallus domesticus). Naturwissenschaften 96, 763–770 (2009). https://doi.org/10.1007/s00114-009-0526-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00114-009-0526-9


